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The Journal of Clinical Endocrinology & Metabolism Vol. 88, No. 3 1319-1322
Copyright © 2003 by The Endocrine Society

Influence of Body Surface Area on Serum Peak Thyrotropin (TSH) Levels after Recombinant Human TSH Administration

Giovanni Vitale, Gelsy Arianna Lupoli, Antonio Ciccarelli, Antonio Lucariello, Maria Rosa Fittipaldi, Francesco Fonderico, Annalisa Panico and Giovanni Lupoli

Dipartimento di Endocrinologia ed Oncologia Molecolare e Clinica (G.V., G.A.L., A.C., M.R.F., F.F., A.P., G.L.), Dipartimento di Medicina Clinica, Scienze Cardiovascolari ed Immunologiche (A.L.), Facoltà di Medicina e Chirurgia, Università degli Studi di Napoli "Federico II", 80127 Napoli, Italy

Address all correspondence and requests for reprints to: Prof. Giovanni Lupoli, Dipartimento di Endocrinologia ed Oncologia Molecolare e Clinica, Università degli Studi di Napoli "Federico II", Via Tasso 113, 80127 Naples, Italy. E-mail: lupoli{at}unina.it or gelsyl{at}hotmail.com.


   Abstract
Top
 Abstract
Introduction
 Patients and Methods
 Results
 Discussion
 References
 
Recombinant human TSH (rhTSH) has been proposed as an alternative method to the withdrawal of thyroid hormones in the follow-up of differentiated thyroid cancer. The aim of the present study was to evaluate the influence of several demographic and anthropometric parameters [age, body weight, height, body mass index, and body surface area (BSA)] on serum peak TSH levels after rhTSH administration.

rhTSH was administered to 112 patients with differentiated thyroid carcinoma according to the conventional two-dose schedule (0.9 mg/d). Serum TSH levels were measured 24 h before and after the first administration of rhTSH, and then 24, 48, and 72 h after the second administration of rhTSH.

In one severely obese patient, serum peak TSH values did not reach a valid stimulation range. Serum peak TSH levels were negatively related to body weight (r = -0.69; P < 0.0001), body mass index (r = -0.51; P < 0.0001), and BSA (r = -0.72; P < 0.0001). In a multivariate regression analysis including demographic and anthropometric variables, only BSA was independently associated to serum peak TSH concentrations (standardized ß coefficient = -0.721; P < 0.0001).

In conclusion, body size seems to influence serum peak TSH levels after rhTSH administration. Future studies should evaluate the possibility of using personalized rhTSH doses, adjusted in relation to BSA.


   Introduction
Top
 Abstract
 Introduction
Patients and Methods
 Results
 Discussion
 References
 
THE POSTSURGICAL FOLLOW-UP of patients with differentiated thyroid cancer includes the evaluation of serum thyroglobulin levels and radioiodine whole body scan. To achieve optimal results, both diagnostic modalities require the stimulation of residual thyroid tissue through high levels of TSH (1, 2, 3).

Until a few years ago, the only methods available to increase TSH levels were either bovine or human (purified from pooled pituitary glands obtained at autopsy) TSH administration and thyroid hormone withdrawal. The use of bovine TSH has been abandoned because of an unacceptably high incidence of side effects (nausea, vomiting, local induration, allergic reactions) and the development of neutralizing antibodies, which restrict its repeated use (4, 5, 6, 7, 8). The use of human cadaver TSH has been limited by the potential transmission of Creutzfeldt-Jakob disease (9, 10). Thyroid hormone withdrawal requires patients to be clinically hypothyroid for several weeks. This condition usually induces a considerable disruption of the patient’s quality of life and work capacity. Besides, the prolonged elevation of serum TSH levels may stimulate the growth of metastatic thyroid disease (11, 12, 13).

These problems have been overcome by the cloning of the gene for the ß-subunit of human TSH and the availability of large quantities of human TSH produced through recombinant DNA technology (14, 15). In fact, the administration of exogenous recombinant human TSH (rhTSH) represents an interesting alternative method to obtain elevated TSH levels (16, 17, 18, 19, 20, 21, 22).

At present, a standard two-dose protocol (0.9 mg/d) is employed for rhTSH administration (17). However, several anthropometric parameters may affect serum TSH levels after rhTSH injection, thus modulating its pharmacokinetics. Therefore, a personalized dose of rhTSH may be required to achieve a potent stimulation.

The current study was undertaken to assess the effectiveness of the standard two-dose protocol for rhTSH in a large cohort of patients and to evaluate the influence of several demographic and anthropometric parameters (age, body weight, height, body mass index, and body surface) on serum peak TSH concentration after rhTSH administration.


   Patients and Methods
Top
 Abstract
 Introduction
 Patients and Methods
Results
 Discussion
 References
 
A total of 112 patients (99 women and 13 men; mean age ± SD, 44.68 ± 14.13 yr) who had previously undergone total thyroidectomy were enrolled in this study. The inclusion criteria were the following: histologically proven differentiated thyroid cancer (84 had papillary carcinoma, and 28 had follicular carcinoma); refusal from the patients to undergo thyroid hormone therapy withdrawal because of the disruptive effects of hypothyroidism, or presence of high risk to induce a metastatic lesion enlargement during thyroid hormone therapy withdrawal, or inability to generate an adequate endogenous TSH response to thyroid hormone withdrawal; no previous administration of exogenous TSH (bovine TSH, cadaver TSH, rhTSH); absence of symptomatic heart disease; absence of significant ascites or other third-space fluid collections; no pregnancy or nursing; normal liver and kidney biochemistry (total bilirubin < 1.5 mg·dl-1, aspartate aminotransferase and alanine aminotransferase less than 3 times the normal limit, prothrombin and partial thromboplastin less than 1.5 times the normal limit, and creatinine less than 1.2 mg·dl-1).

All patients were treated with levothyroxine (1.5–2.5 µg/kg body weight) to achieve TSH levels lower than 0.1 mIU/liter. A dose of 0.9 mg of rhTSH was injected im for 2 consecutive days according to the conventional schedule (17 ). rhTSH (Thyrogen, Genzyme, Cambridge, MA) was produced as previously described (19).

Blood samples were taken for the dosage of TSH 24 h before and after the first administration of rhTSH, as well as 24, 48, and 72 h after the second administration of rhTSH. Serum TSH was evaluated using an immunochemiluminometric assay (LIAISON TSH, Byk Gulden Italia, Milan, Italy) with a functional sensitivity less than 0.02 mIU/liter, an analytical sensitivity less than 0.004 mIU/liter, an intra-assay precision of 1.9% at 0.17 mIU/liter and 0.9% at 36.1 mIU/liter, and an interassay precision of 5.1% at 0.17 mIU/liter and 2.2% at 36.8 mIU/liter. TSH parameters have been evaluated by performing each serum specimen at two dilutions (undiluted and 1:10) to avoid hook effects. All TSH measurements were performed twice, and all samples from a given subject were evaluated in the same assay.

At the beginning of the study, body weight and height were measured by standard technique to the nearest 0.1 kg and 0.01 m, respectively; body mass index (BMI) was calculated as weight/height squared (kg/m2); body surface area (BSA) was measured according to the Haycock’s formula (24.265 x 10-3 x height0.3964 x weight0.5378), where height was expressed in centimeters, weight in kilograms, and BSA in square meters (23).

All patients gave written informed consent regarding the use of rhTSH and the taking of several blood samples, as previously reported.

Data are presented as mean value ± SD. Univariate relations were assessed by Pearson’s method. Stepwise forward multiple linear regression test was performed for multivariate analysis. The level of significance was P value less than 0.05.


   Results
Top
 Abstract
 Introduction
 Patients and Methods
 Results
Discussion
 References
 
The characteristics of the study population are summarized in Table 1Go. The mean age was 44.68 ± 14.13 yr, and the overall population included 3 children under 12. In addition, 14 of 112 patients were obese (BMI >= 30 kg/m2) and 4 of 112 were underweight (BMI < 18.5 kg/m2).


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  		Table 1. Characteristics of the study population

 
Before rhTSH administration, TSH levels were suppressed to 0.0150 ± 0.0222 mIU/liter. After rhTSH administration, mean serum peak TSH concentration was 120.25 ± 46.79 mIU/liter. The TSH levels were in a potent stimulation range (>=30 mIU/liter) in 111 of 112 patients. In one patient, serum peak TSH value after rhTSH injections was inadequate to perform radioiodine whole body scan (TSH, 22 mIU/liter). This patient presented severe obesity (BMI, 41.52 kg/m2; body weight, 120 kg; BSA, 2.44 m2). One hundred five of 112 patients showed serum peak TSH levels ranging from 30–200 mIU/liter. In six cases, serum peak TSH values were higher than 200 mIU/liter. Two of these six patients were adults with normal or mildly increased BMI (age, 69 and 66 yr, respectively; BMI, 21.49 and 25.65 kg/m2, respectively; BSA, 1.57 and 1.80 m2, respectively), another two patients were underweight (age, 28 and 53 yr, respectively; BMI, 15.23 and 16.18 kg/m2, respectively; BSA, 1.40 and 1.52 m2, respectively), and two patients were children (age, 10 and 11 yr, respectively; BMI, 22.28 and 22.45 kg/m2, respectively; BSA, 1.23 and 1.32 m2, respectively). In another child under 12 yr old, serum peak TSH and BSA values were 180 mIU/liter and 1.46 m2, respectively.

Univariate relations of serum peak TSH concentrations with body weight, height, BMI, BSA, and age were tested in the overall population. TSH was negatively related to weight (r = -0.69; P < 0.0001), BMI (r = -0.51; P < 0.0001), and BSA (r = -0.72; P < 0.0001; Fig. 1Go), but not to height or age.



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  		Figure 1. Inverse relation between BSA and serum peak TSH after rhTSH administration.

 
In a multiple linear regression analysis (Table 2Go), performed to assess independent associations of serum peak TSH concentrations and including age, height, weight, BMI, and BSA as potential determinants, only BSA (standardized ß coefficient = -0.721; P < 0.0001) was independently associated to serum peak TSH levels.


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  		Table 2. Multiple linear regression analysis with serum peak TSH concentrations as dependent variable

 
The treatment was well tolerated. Of the 112 study patients, 101 (90.2%) showed no adverse effects. Three patients experienced mild nausea, moderate headache occurred in four patients, one patient with brain metastases referred a severe headache, and three patients with bone metastases reported severe skeletal pain. In three of the symptomatic four patients with metastases, serum peak TSH levels after rhTSH administration were higher than 200 mIU/liter, whereas serum peak TSH values ranged from 39–180 mIU/ml in seven patients without metastases showing mild nausea and moderate headache. In these seven patients, the occurrence of symptoms was not significantly related to TSH levels.


   Discussion
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Discussion
References
 
It has been demonstrated that the two-dose rhTSH regimen represents an optimum protocol to induce radioiodine uptake and thyroglobulin secretion during the follow-up of differentiated thyroid carcinoma (17). This procedure consists in the administration of 0.9 mg rhTSH im for 2 consecutive days. Twenty-four hours after the last rhTSH injection (third day), a tracer dose of radioiodine (4–5 mCi) is administered. Serum thyroglobulin dosage and whole body scanning are performed on the fifth day. Whole body scans performed after rhTSH showed high concordance with scans after the withdrawal of thyroid hormone therapy in detecting locoregional and/or distant metastases. In addition, the use of rhTSH is safe and well tolerated. It allows the continuation of thyroid hormone therapy and avoids the debilitating symptoms of hypothyroidism (16, 17, 18, 19, 20, 21, 22, 24, 25).

In the present study, an inadequate increase in TSH after a two-dose rhTSH administration has been observed in one patient affected by severe obesity (BMI >= 40 kg/m2). On the other hand, in six patients the serum peak TSH levels were higher than 200 mIU/liter. These levels were considerably higher than normally required. Although the administration of rhTSH induced an increase in serum TSH values for a short time, thus avoiding a prolonged stimulation of metastases, the possibility that tumor growth was accelerated by rhTSH in patients with very high serum TSH levels cannot be dismissed. In fact, it has been recently observed that rhTSH may stimulate tumor mass with consequent tumor swelling (16, 26, 27, 28). Braga et al. (26) reported two cases with papillary thyroid carcinoma and local recurrent tumor. Both patients developed a sudden enlargement of tumor mass 12–48 h after the second rhTSH administration. In one patient, the serum TSH level after rhTSH injection was 216 mIU/liter. Vargas et al. (27) described a hypopituitary patient with follicular thyroid carcinoma metastatic to the brain who developed hemiplegia 24 h after the second rhTSH injection. Also in this case, serum TSH concentration reached excessively high levels (572 mIU/liter). Robbins et al. (28) reported the occurrence of confusion, ataxia, dysphagia, headache, and papilledema 24 h after the second rhTSH injection in a patient with follicular carcinoma and brain metastases. According to the manufacturer (29), 4 of 55 patients with brain metastases experienced acute hemiplegia, hemiparesis, or headache 1–3 d after rhTSH administration, attributed to edema or focal hemorrhage within the tumor. In addition, one case of acute visual loss and one of severe dysphagia have been reported 1 d after rhTSH injection in patients with metastases to the optic nerve and paratracheal areas, respectively. In addition, Lippi et al. (30) reported the occurrence of transient swelling and pain at the metastatic site after rhTSH administration in two patients with bone metastases from thyroid cancer. Therefore, rhTSH has overcome some of the problems related to the risk of tumor growth, thanks to the short time of action. However, very high levels of TSH could stimulate tumor mass, although it acts for a short time.

In the present study, we described the occurrence of severe headache in one patient with brain metastases and violent skeletal pain in three patients with bone metastases after rhTSH administration. In three of these four patients, serum peak TSH after rhTSH administration was higher than 200 mIU/liter. Therefore, it is very important to reach serum TSH levels ranging between 30 and 200 mIU/liter after rhTSH administration to obtain an adequate uptake of radioiodine, thus avoiding an excessive stimulation of tumor mass.

The negative linear correlation between serum peak TSH concentration and several anthropometric parameters (body weight, BMI, and BSA) suggests that the entity of rhTSH stimulation may be influenced by body size, particularly by BSA, as confirmed by multivariate analysis. These relations could explain the inadequate increase of TSH serum levels after rhTSH administration in one patient with high BSA (2.44 m2) and the extremely high serum peak TSH levels in patients with low BSA (BSA values were equal to or lower than 1.57 m2 in five of six patients with TSH > 200 mIU/liter).

On this basis, a personalized rhTSH dose, adjusted for BSA, should be used in clinical practice. Future studies should clarify the appropriate dosage of rhTSH, adjusted for BSA, to be administered in patients with differentiated thyroid carcinoma to obtain optimal TSH values.


   Acknowledgments
 
We thank Granata Gabriella and Sands Philip for help in preparation of the manuscript and Cuomo Clelia, Di Francia Angelo, Di Guida Annamaria, Salvatore Luisa, and Vastarella Giuseppe for skillful technical assistance.


   Footnotes
 
Abbreviations: BMI, Body mass index; BSA, body surface area; rhTSH, recombinant human TSH.

Received June 20, 2002.

Accepted November 26, 2002.


   References
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Discussion
 References
 

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